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Hypercarnivory and the brain: protein requirements of cats reconsidered

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Abstract

The domestic hypercarnivores cat and mink have a higher protein requirement than other domestic mammals. This has been attributed to adaptation to a hypercarnivorous diet and subsequent loss of the ability to downregulate amino acid catabolism. A quantitative analysis of brain glucose requirements reveals that in cats on their natural diet, a significant proportion of protein must be diverted into gluconeogenesis to supply the brain. According to the model presented here, the high protein requirement of the domestic cat is the result of routing of amino acids into gluconeogenesis to supply the needs of the brain and other glucose-requiring tissues, resulting in oxidation of amino acid in excess of the rate predicted for a non-hypercarnivorous mammal of the same size. Thus, cats and other small hypercarnivores do not have a high protein requirement per se, but a high endogenous glucose demand that is met by obligatory amino acid-based gluconeogenesis. It is predicted that for hypercarnivorous mammals with the same degree of encephalisation, endogenous nitrogen losses increase with decreasing metabolic mass as a result of the allometric relationships of brain mass and brain metabolic rate with body mass, possibly imposing a lower limit for body mass in hypercarnivorous mammals.

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Acknowledgments

Much of the work on an earlier draft of this paper was done while I was a fellow at the Smithsonian National Zoological Park, and I thank J. Seidensticker for his encouragement and support of this endeavour. I also wish to thank S. Lumpkin and M. Power for commenting on an earlier version of the manuscript, and J. Noordhof and in particular O. Oftedal for critical discussions of the subject matter. I also thank my anonymous reviewers, D. Millward and especially G. Lobley for their time and constructive comments. This work was supported by a grant from the National Science Foundation-Office of Polar Programs No. 0538592.

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Communicated by I.D. Hume.

Appendix: Total carbohydrate in a mouse

Appendix: Total carbohydrate in a mouse

The calculation presented here was intentionally done as a ‘best-case scenario’ to estimate the maximal amount of digestible carbohydrate a cat could derive from consuming gut contents of small, granivorous rodent prey. Data used in the calculation include body composition of Swiss albino mice (Bailey et al. 1960) and mouse gut volumes from Cizek (1954). Mice were chosen because they are granivorous rather than herbivorous, have a relatively large gut volume (Cizek 1954), and body composition data are readily available. It is assumed that gut contents consist entirely of finely ground whole wheat grain (composition of dry matter: 11.2% fibre, 73.9% starch and dextrins, 2.6% sugars: Paul and Southgate 1978), and that digestibility of starch in gut contents is 97.2% in cats (Morris et al. 1977). It is further assumed that cats cannot digest non-starch polysaccharides to a significant extent (NRC 2006) but that simple sugars are completely digested. BM, body mass.

Glycogen in liver and muscle

  1. (a)

    Liver mass and glycogen content

    • Liver mass of adult mice = ca. 5% of body mass (Von Ehrenstein 1958; Barnett and Widdowson 1965; Chaffee et al. 1966).

    • Liver glycogen content in mice (Ryder et al. 1999): 100–400 μmol glucose g−1 liver wet mass, equivalent to 1.8–7.2 g glucose 100 g−1 liver.

  2. (b)

    Skeletal muscle mass and glycogen content

    • Skeletal muscle mass in rats is ca. 64% of lean body mass and ca. 45% of BM (Even et al. 2001); this is consistent with ash-free, fat-free carcass mass (an approximation of total skeletal muscle mass) in mice of ca. 44% of BM (Corva and Medrano 2000).

    • Muscle glycogen content (Ryder et al. 1999): 20 μmol glucose g−1 wet muscle, 0.4 g glucose 100 g−1 wet muscle.

    • Please note that mouse muscle contains considerably less glycogen than human muscle tissue (0.2–0.4 vs. 2%).

Combining (a) and (b):

Assume mouse 22 g, 14% body fat, 18.92 g lean mass

Approximate liver mass (5% BM)

1.1 g

Glycogen in liver (7%)

77 mg

Muscle mass (45% of BM)

9.9 g

Glycogen in muscle (0.4%)

40 mg

Total glycogen

0.124 g

Digestible carbohydrate in the digestive tract of prey

Body mass mouse

22 g

Gut contents (DM)

0.30 g

 73.8% starch + dextrins

0.219 g

 ×0.972

0.212 g

Sugars, 2.6%

0.008 g

Total available CHO

0.220 g

3.69 kJ

Summary: total carbohydrate (CHO)

Glycogen in liver and muscle (see also Table 2)

0.124 g

Available carbohydrate in gut contents (above)

0.220 g

Total available CHO (×16.76 kJ g−1)

0.344 g

5.76 kJ

Total ME of mouse (see Table 2)

8.60 kJ g−1

188.3 kJ

Carbohydrate as %ME

(5.76/188.3) × 100 = 3.1%

In 6 mice (equivalent to daily ME)

 Total ME

1,135.2 kJ

 ME from carbohydrate

34.6 kJ

 Total carbohydrate

2.1 g

Even in the best-case scenario presented here, consumption of gut contents would contribute insufficient glucose equivalents to meet estimated whole-body carbohydrate demand (the brain alone consumes ca. 3 g glucose day−1; Table 4), assuming that cats actually consume gut contents. Prey larger than mice, such as rabbits, tend to be herbivorous rather than granivorous and possess fermentative digestion; it is questionable whether cats would consume partially digested herbage and if they did, it is unlikely cats could derive significant carbohydrate from this source. In general, neither cats (Leyhausen 1979) nor large felids such as tigers (Panthera tigris) and mountain lions (Puma concolor) consume the gut contents of their prey (J. Seidensticker, pers. comm., 01 June 2009).

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Eisert, R. Hypercarnivory and the brain: protein requirements of cats reconsidered. J Comp Physiol B 181, 1–17 (2011). https://doi.org/10.1007/s00360-010-0528-0

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